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Regurgitant Derived From the Tea Geometrid Ectropis obliqua Suppresses Wound-Induced Polyphenol Oxidases Activity in Tea Plants

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Abstract

Polyphenol oxidases (PPOs) have been reported to play an important role in protecting plants from attack by herbivores. However, little is known about their role in tea. Here, we investigated the effect of PPOs on interactions between tea plants and the tea geometrid Ectropis obliqua, one of the most important insect pests of tea. Jasmonic acid (JA) treatment resulted in increases in PPO activity, and the effect of JA was dose dependent. Ectropis obliqua caterpillars grew and developed more slowly on JA-treated tea plants than on control plants, and larval weight gains depended on the JA dosage. Artificial diet complemented with PPOs reduced the growth and survival rate of E. obliqua caterpillars, and there was a negative relationship between PPO level and larval growth and survival. Unlike mechanical wounding, which is an effective inducer of tea plant PPO activity, wounding plus the herbivore regurgitant or herbivore infestation suppressed the wound-induced PPO activities, especially at 4 days after treatment. These results suggest that PPOs are an important anti-herbivore factor in tea plants, defending them against E. obliqua larvae, and that E. obliqua larvae have evolved to elude the tea plant’s defense by inhibiting the production of PPOs.

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References

  • Barbehenn RV, Jones CP, Yip L, Tran L, Constabel CP (2007) Limited impact of elevated levels of polyphenol oxidase on tree-feeding caterpillars: assessing individual plant defenses with transgenic poplar. Oecologia 154:129–140

    Article  PubMed  Google Scholar 

  • Becklin KM (2008) A coevolutionary arms race: understanding plant-herbivore interactions. Am Bio Teach 5:288–292

    Article  Google Scholar 

  • Bede J, Musser R, Felton G, Korth K (2006) Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terponoid biosynthesis. Plant Mol Biol 60:519–531

    Article  PubMed  CAS  Google Scholar 

  • Berenbaum M (1980) Adaptive significance of midgut pH in larval Lepidoptera. Am Nat 115:138–146

    Article  Google Scholar 

  • Bhonwong A, Stout MJ, Attajarusit J, Tantasawat P (2009) Defensive role of tomato polyphenol oxidases against cotton bollworm (Helicoverpa armigera) and beet armyworm (Spodoptera exigua). J Chem Ecol 35:28–38

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Castañera P, Steffens JC, Tingey WM (1996) Biological performance of Colorado potato beetle larvae on potato genotypes with differing levels of polyphenol oxidase. J Chem Ecol 22:91–101

    Article  Google Scholar 

  • Chakraborty U, Chakraborty N (2005) Impact of environmental factors on infestation of tea leaves by Helopeltis theivora, and associated changes in flavonoid flavor components and enzyme activities. Phytoparasitica 33:88–96

    Article  CAS  Google Scholar 

  • Chen YG, Huang MD (2001) Bioloical control progress of Ectropis obliqua Prout. Nat Enemies Insects 23:181–184

    Google Scholar 

  • Constabel CP, Ryan CA (1998) A survey of wound- and methyl jasmonate-induced leaf polyphenol oxidase in crop plants. Phytochemistry 47:507–511

    Article  CAS  Google Scholar 

  • Constable CP, Bergey DR, Ryan CA (1995) Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci USA 92:407–411

    Article  CAS  Google Scholar 

  • Constable CP, Bergey DR, Ryan CA (1996) Polyphenol oxidase as a component of the inducible defense response in tomato against herbivores. In: Romeo JT, Saunders JA, Barbosa P (eds) Phytochemical diversity and redundancy in ecological interactions. Plenum, New York, pp 231–252

    Google Scholar 

  • Constable CP, Yip L, Patton JJ, Christopher ME (2000) Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiol 124:285–295

    Article  Google Scholar 

  • Dam V, Horn M, Mares M, Baldwin IT (2001) Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. J Chem Ecol 3:547–568

    Google Scholar 

  • Duffey SS, Stout MJ (1996) Antinutritive and toxic compounds of plant defense against insects. Arch Insect Biochem Physiol 32:3–37

    Article  CAS  Google Scholar 

  • Eichenseer H, Mathews MC, BI JL, Murphy JB, Felton GW (1999) Salivary glucose oxidase: multifultional roles for Helicoverpa zea. Arch Insect Biochem 42:99–109

    Article  CAS  Google Scholar 

  • Felton GW, Eichenseer H (1999) Herbivore saliva and its effect on plant defense against herbivores and pathogens, in induced plant defenses against pathogens and herbivores. The American Phytopathological Society Press, St. Paul

    Google Scholar 

  • Felton GW, Donato RJ, Vecchio D, Duffey SS (1989) Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J Chem Ecol 15:2667–2694

    Article  CAS  Google Scholar 

  • Felton GW, Donato KK, Broadway RM, Duffey SS (1992) Impact of oxidized plant phenolics on the nutritional quality of dietary protein to a noctuid herbivore. Spodoptera exigua. J Insect Physiol 38:277–285

    Article  CAS  Google Scholar 

  • Gershenzon J, Wolfgang K (1999) Biochemistry of terpenoids. In: Michael W (ed) Biochemistry of plant secondary metabolism. Sheffield Academic Press, London, pp 222–279

    Google Scholar 

  • He JP, Chen FD, Chen SM, Lu GS, Deng YM, Fang WM, Liu ZL, Guan ZY, He CY (2011) Chrysanthemum leaf epidermal surface morphology and antioxidant and defense enzyme activity in response to aphid infestation. J Plant Physiol 7:687–693

    Article  CAS  Google Scholar 

  • Jin SY, Hong JH (1999) Effects of wounding and jasmonic acid on polyphenol oxidase in tomato seedlings. J Environ Sci-China 669–676

  • Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 6:1008–1019

    Article  CAS  Google Scholar 

  • Lawrence SD, Novak NG, Blackburn MB (2007) Inhibition of proteinase inhibitor transcripts by Leptinotarsa decemlineata regurgitant in Solanum lycopersicum. J Chem Ecol 33:1041–1048

    Article  PubMed  CAS  Google Scholar 

  • Mahanil S, Attajarusit J, Stout MJ, Thipyapong P (2008) Overexpression of tomato polyphenol oxidase increases resistance to common cutworm. Plant Sci 174:456–466

    Article  CAS  Google Scholar 

  • Mayer AM (1987) Polyphenol oxidase in plants-recent progress. Phytochemistry 26:11–20

    Article  Google Scholar 

  • Mayer AM (2006) Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67:2318–2331

    Article  PubMed  CAS  Google Scholar 

  • Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Caterpillar saliva beats plant defenses: a new weapon emerges in the coevolutionary arms race between plants and herbivores. Nature 416:599–600

    Article  PubMed  CAS  Google Scholar 

  • Ohnmeiss TE, Baldwin IT (2000) Optimal defense theory predicts the ontogeny of an induced nicotine defense. Ecology 7:1765–1783

    Article  Google Scholar 

  • Pinto MST, Siqueira FP, Oliverira AEA, Fernandes KVS (2008) A wounding-induced PPO from cowpea (Vigna unguiculata) seedlings. Phytochemistry 69:2297–2302

    Google Scholar 

  • Raj SN, Sarosh BR, Shetty HS (2006) Induction and accumulation of polyphenol oxidase activities as implicated in development of resistance against pearl millet downy mildew disease. Funct Plant Biol 33:563–571

    Article  CAS  Google Scholar 

  • Ren F, Lu YT (2006) Overexpression of tobacco hydroxyproline-rich glycopeptide systemin precursor. A gene in transgenic tobacco enhances resistance against Helicoverpa armigera larvae. Plant Sci 171:286–292

    Article  CAS  Google Scholar 

  • Schwartzberg EG, Böröczky K, Tumlinson JH (2011) Pea aphids, Acyrthosiphon pisum, suppress induced plant volatiles in broad bean, Vicia faba. J Chem Ecol 37:1055–1062

    Google Scholar 

  • Shi C, Dai Y, Xu X, Xie Y, Liu Q (2002) The purification of polyphenol oxidase from tobacco. Protein Exp Purif 24:51–55

    Article  CAS  Google Scholar 

  • Steffens JC, Harel E, Hunt MD (1994) Polyphenol oxidase. In: Ellis BE, Kuroki GW, Stafford HA (eds) Genetic engineering of plant secondary metabolism. Plenum, New York, pp 276–304

    Google Scholar 

  • Sun XL, Cai XM, Ma CL, Wang GC, Chen ZM (2011) Kinetics of polyphenol oxidase activity in tea leaves induced by exogenous application of MeJA and mechanical damage. Acta Bot Boreal-Occident Sin 9:1805–1810

    Google Scholar 

  • Thaler JS, Fidantsef AL, Duffey SS, Bostock RM (1999) Trade-offs in plant defense against pathogens and herbivores: a field demonstration of chemical elicitors of induced resistance. J Chem Ecol 25:1597–1609

    Article  CAS  Google Scholar 

  • Thaler JS, Karban R, Ullman DE, Boege K, Bostock RM (2002) Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131:227–235

    Article  Google Scholar 

  • Thipyapong P, Steffens JC (1997) Tomato polyphenol oxidase (Differential response of the polyphenol oxidase F promoter to injuries and wound signals). Plant Physiol 2:409–418

    Google Scholar 

  • Wang GC (2010) Ecological functions of tea plant volatiles induced by three herbivores. Ph.D. dissertation. The Chinese Academy of Agricultural Sciences

  • Wang J, Constabel CP (2004) Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta 220:87–96

    Article  PubMed  CAS  Google Scholar 

  • Wang X, HU LC, ZHOU GX, CHENG JA, LOU YG (2011) Salicylic acid and ethylene signaling pathways are involved in the production of the rice trypsin proteinase inhibitors induced by the leaf folder Cnaphalocrocis medinalis (Guenée). Chin Sci Bull 22:2351–2358

    Article  CAS  Google Scholar 

  • Winde I, Wittstock U (2011) Insect herbivore counter adaptations to the plant glucosinolate–myrosinase system. Phytochemistry 13:1566–1575

    Article  CAS  Google Scholar 

  • Zeier J (2005) Age-dependent variations of local and systemic defense responses in Arabidopsis leaves towards an avirulent strain of Pseudomonas syringae. Physiol Mol Plant P 66:30–39

    Article  CAS  Google Scholar 

  • Zong N, Wang C (2004) Induction of nicotine in tobacco by herbivory and its relation to glucose oxidase activity in the labial gland of three noctuid caterpillars. Chin Sci Bull 49:1596–1601

    CAS  Google Scholar 

Download references

Acknowledgments

We thank Emily Wheeler for editorial assistance. The study was sponsored by National Program on Key Basic Research Project (973 Program) (2012CB114104), National Natural Science Foundation of China (31272053; 31171862), and the Division of Science and Technology of Zhejiang Province (2011C22043).

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Authors and Affiliations

  1. Tea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, 310008, China

    Zi-Wei Yang, Xiao-Na Duan, Shan Jin, Xi-Wang Li, Zong-Mao Chen & Xiao-Ling Sun

  2. Northeast Normal University, Changchun, 130024, China

    Xiao-Na Duan & Bing-Zhong Ren

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  1. Zi-Wei Yang
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  2. Xiao-Na Duan
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  3. Shan Jin
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  4. Xi-Wang Li
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  5. Zong-Mao Chen
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  7. Xiao-Ling Sun
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Correspondence to Xiao-Ling Sun.

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Zi-Wei Yang and Xiao-Na Duan contributed equally.

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Fig. S1

Mean absorbance (±SE) for the production of tea sustract, catechins, and artificial diet that catalyzed by mushroom PPO in different concentrations. Duncan’s multiple range test: capitalization letters P<0.001; lowercase P<0.05. (PDF 13 kb)

Fig. S2

Mean absorbance (±SE) for the production of catechins and artificial diet that catalyzed by tea extract in different concentrations. t-test: *P<0.05. (PDF 11 kb)

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Yang, ZW., Duan, XN., Jin, S. et al. Regurgitant Derived From the Tea Geometrid Ectropis obliqua Suppresses Wound-Induced Polyphenol Oxidases Activity in Tea Plants. J Chem Ecol 39, 744–751 (2013). https://doi.org/10.1007/s10886-013-0296-x

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  • DOI: https://doi.org/10.1007/s10886-013-0296-x

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